Role of hydrogen and metals Role of hydrogen and metals in the formation and evolution in the formation and evolution

metabolic systemsmetabolic systems

Mikhail Fedonkin

Geological Institute, Russian Academy

of Sciences, Moscow

Oparin-2014The problem of the origin of life

Moscow, September 22-26, 2014

Alexander Ivanovich Oparin, 1894-1980, biochemist, author of the theory of the origin of life:

Oparin, A. I. The Origin of Life. Moscow: Moscow Worker publisher, 1924.

According to Oparin the early Earth had a strongly reducing atmosphere, containing hydrogen, water vapor, methane, and ammonia.

These elements and simple compounds were the raw materials for complex organic molecules subjected to natural selection and evolution.

Georges Cuvier, 1769 - 1832

Tornado, Cuvier’s metaphor for life: priority of energy flow

Nonequilibrium, - the flow of matter or energy, Nonequilibrium, - the flow of matter or energy, can be the source of order and complexity can be the source of order and complexity (Prigogine and Stengers, 2003) (Prigogine and Stengers, 2003)

Morowitz, 1992

Origin of life: physical approach priority

In the contrast to the chemical approach focused on the origin of “building blocks” of the living cell (RNA, DNA, proteins etc.),

the physical approach concentrates on the origin of energy flow common for all living organisms: proton gradients and electron transfer.

Central place should belong to hydrogen and metals!

Wackett et al., 2004

В начале был единый Океан,В начале был единый Океан,Дымившийся на раскаленном ложе.Дымившийся на раскаленном ложе.И в этом жарком лоне завязалсяИ в этом жарком лоне завязалсяНеразрешимый узел жизни: плоть,Неразрешимый узел жизни: плоть,Пронзенная дыханьем и биеньем.Пронзенная дыханьем и биеньем.Планета стыла.Планета стыла.Жизни разгорались.Жизни разгорались.Наш пращур, что из охлажденных водНаш пращур, что из охлажденных водСвой рыбий остов выволок на землю,Свой рыбий остов выволок на землю,В себе унес весь древний ОкеанВ себе унес весь древний ОкеанС дыханием приливов и отливов,С дыханием приливов и отливов,С первичной теплотой и солью вод —С первичной теплотой и солью вод —Живую кровь, струящуюся в жилах.Живую кровь, струящуюся в жилах.

In the beginning there was a single ocean,In the beginning there was a single ocean,That was smoking on the heated bed.That was smoking on the heated bed.And in this hot lap ensuedAnd in this hot lap ensuedInsoluble knot of life: the flesh,Insoluble knot of life: the flesh,Pierced by breath and beat.Pierced by breath and beat.The planet cooled.The planet cooled.Lives flared.Lives flared.Our ancestor that of chilled waterOur ancestor that of chilled waterHis fish skeleton dragged to the ground,His fish skeleton dragged to the ground,In itself carried all the ancient oceanIn itself carried all the ancient oceanWith the breath of the tides,With the breath of the tides,With the primary heat and salt of water -With the primary heat and salt of water -Live blood flowing in his veins.Live blood flowing in his veins.

1877-19321877-1932

Concentration of metalsConcentration of metalsin human plasma and in human plasma and in sea waterin sea water ((nmnm//ll))

Fe 22300 / 0,5-20 Zn 17200 / 80 Cu 16500 / 10Mo 10000 / 100 Cr 55 / 4 V 200 / 40 Mn 110 / 0,7 Ni 44 / 5

Fe – 87 000 Fe – 87 000 Zn – 65 000 Zn – 65 000 Al – 25 000Al – 25 000N – 19 000 N – 19 000 P – 15 000P – 15 000Cu – 17 000 Cu – 17 000 Mn – 9 400Mn – 9 400Cd – 910Cd – 910S – 1.7S – 1.7Mg – 0.69 Mg – 0.69 Na – 0.14Na – 0.14

Ratio of the concentration of elements in phytoplankton to concentration of elements in sea water reflects the degree of biological need and, on the other hand, the degree of depletion of the particular elements from the seawater Bowen (1966)

Phytoplankton Phytoplankton vsvs sea water sea water chemistrychemistry

Biologically relevant metalsBiologically relevant metals Na, K, Ca, Mg, Mn, Zn, Cu, Fe,

V, Cr, Co, Ni, Mo, W

Metals in the living cell serve as– electron-transfer agents– oxygen carriers– cellular messengers– structural components of proteins– nucleophiles– catalysts

Some specific metal ion catalysis

Frausto da Silva & Williams, 1997

over 30% of known enzymes contain metal ions as a cofactor of an active site

metal activators increase the rate of reactions catalysed by enzymes up 1012 times!

removal of the metals from protein molecule leads to

decrease or loss of its catalytic properties.

Transition metals as catalystsTransition metals as catalysts

Could the metals ions or their simple compounds be the first catalysers that, due to fast reactions segregated life, first dynamically and then structurally, from the mineral realm?

At catalytic centres, metals increase acidity, electrophilicity At catalytic centres, metals increase acidity, electrophilicity and/orand/or nucleophilicity of reacting species, promote heterolysis, nucleophilicity of reacting species, promote heterolysis, or receiveor receive and donate electrons. and donate electrons.

The protein’s primary and secondary The protein’s primary and secondary mmetalcoordinationetalcoordination spheres spheres tune the properties of the metal to optimizetune the properties of the metal to optimize reactivity and reactivity and influence metal selection. influence metal selection.

Donor ligands (S, O or N) canDonor ligands (S, O or N) can impart bias in favour of the impart bias in favour of the correct metal.correct metal.

Crystal structure of the nitrogenase MoCrystal structure of the nitrogenase Mo--Fe proteinFe protein..Are the proteins the later addition to the primary Are the proteins the later addition to the primary inorganic catalysts? inorganic catalysts?

The elements used as cofactors by enzymes are shown in blue. The height of each column represents the proportion of all enzymes with known structures using the respective metal. A single enzyme uses cadmium(Waldron et al., 2009).

The proportion of proteins using the indicated metalsthat occur in each of the six Enzyme classes: oxidoreductases (EC 1), blue;transferases (EC 2), yellow; Hydrolases (EC 3), purple; lyases (EC 4), pink;isomerases (EC 5), green; Ligases (EC 6), grey.

EC, Enzyme Commission.

After Waldron et al., 2009

The abundances of Fe-, Zn-, Mn-, and CoB12-binding structural domains in the proteomes of Archaea (black), Bacteria (red), and Eukarya (blue). Dupont et al., 2009

Occurrence of Cu users and nonusers among bacteria differing in their dependence on oxygen (Ridge et al., 2008).

Cu

Bacteria

Occurrence of Cu users and nonusers among archaea differing in their dependence on oxygen (Ridge et al., 2008).

Cu

Archaea

Taxonomic and ecological distribution of the Taxonomic and ecological distribution of the metals as activators of enzymes may be a metals as activators of enzymes may be a subject for geohistorical and evolutionary subject for geohistorical and evolutionary interpretation. interpretation.

Hydrogen role in the energetic Hydrogen role in the energetic metabolismmetabolism

Hydrogen, the most abundant chemical element in the Universe, well could be the primary fuel for early life.

Biological role of hydrogen is related not only to the domination of H2O in the mass of the living cell.

The soft hydrogen bonds provide stability and versatility of the macromolecules.

Many recent microorganisms use H2 as a source of energy.

Hydrogen role in the energetic Hydrogen role in the energetic metabolismmetabolism

Various microbial enzymes perform the H+ transfer. The H+ gradients are used in the process of ATP

generation. Negative ion of hydrogen H- is known as an energy

currency of the cell (an equivalent of two electrons).

H2 as a key intermediate product of anaerobic metabolism makes a universal trophic (energetic) connection between the microorganisms that live on different substrates – a key ecosystem factor.

Biological role of hydrogenBiological role of hydrogen

Many microorganisms use H2 as an electron donor in both catabolic and anabolic redox processes.

H2 plays an important role as an intermediary metabolite during microbial transformation of organic matter.

H2 is produced as a catabolic end product by a variety of anaerobic bacteria or as a byproduct of the nitrogenase reaction by nitrogen-fixing bacteria.

Biological role of hydrogenBiological role of hydrogen

Anaerobically, hydrogen oxidation is coupled to CO2 reduction by methanogens and acidogens, and to sulfate reduction by sulfidogenic bacteria.

Aerobically, the hydrogen bacteria use hydrogen gas for both energy conservation and autotrophic CO2 fixation.

Phototrophic bacteria can either produce or consume molecular hydrogen.

Biological role of hydrogen Biological role of hydrogen

Hydrogen as a source of energy and free electrons is easy to take up by various chemosynthesizing organisms.

The near universality of hydrogen metabolism among microorganisms and high similarity between all the Ni-Fe hydrogenase operons suggests that the microbial ability to metabolize hydrogen is of great importance and ancient origin (Casalot, 2003).

Hydrogen metabolism in BacteriaHydrogen metabolism in Bacteria

Proportions of the H2 oxidizing methanogenic Archaea (99%) and Bacteria in groundwater from Lidy Hot Spring (Beaverhead Mts, Idaho).Depth 200 m, temperature 58.5 °C, anoxic, very low dissolved Corg and high concentration of H2 (Chapelle et al., 2002).

Spear et al., 2006

Stetter, 1996

Hyperthermophyles

O2

H2

Fundamental differencebetween prokaryotic and eukaryotic physiology from the standpoint of energy metabolism may indicate chemoautotrophic origin of life.

Large part of the reactions in the prokaryotes involveshydrogen and its volatilecompounds that must bethe primary feature.

Redox reactions involving inorganic donors and acceptors after Amend & Shock, 2001,Doeller et al. 2001 (see refs. in Martin & Russell, 2002)

EUBACTERIA

ARCHAEOBACTERIA

EUKARYOTES

The prime role of hydrogen and its close interactions with otherestablished biogeochemical cycles (Williams & Ramsden 2007)

catalysts

The role of hydrogen and the connection that it forms between the geological world and thebiological world (Nealson, 2005)

The deep hydrogen-driven biosphere hypothesis (Karsten, Pedersen, 2000)

Early Earth (> 4 Ga)Early Earth (> 4 Ga)

Radiogenic heat was over 10 times higher than Radiogenic heat was over 10 times higher than at presentat present

Contribution of close Moon into the mechanical Contribution of close Moon into the mechanical heating of the Earth interior was highheating of the Earth interior was high

Intensive volcanism Intensive volcanism Full recycling of the earth crustFull recycling of the earth crust Low reliefLow relief Global shallow oceanGlobal shallow ocean

400C springs

Russell & Hall 2006 GSA Mem192, 1-32

1-10 bars CO2

ocean ocean ocean

CO2CO2

CO2

Mantle convection cells at 4.4Ga

Early Earth (> 4 Ga)Early Earth (> 4 Ga)

Low luminosity of Sun Low luminosity of Sun (30% (30% below present)below present) Dense green-house atmosphereDense green-house atmosphere High temperature of the planet surfaceHigh temperature of the planet surface Rapid formation of the metal core of the planet Rapid formation of the metal core of the planet

(during the first 100 Ma)(during the first 100 Ma) Magnetic field was established early as wellMagnetic field was established early as well Reducing atmosphereReducing atmosphere Anoxia, no protective ozone screenAnoxia, no protective ozone screen

Hydrothermal mounds were key to life’s origin. Alkaline fluids from such vents carried hydrogen, sulfide and ammonia. Water was enriched with the heavy metals (Fe, Ni etc.).

Iron sulfide bubbles around alkaline vents in the Hadean ocean. Fe-Ni sulfides catalyzed synthesis of simple organic molecules that formed more complex peptides. The peptides have coated the inside surfaces of the bubbles, the first step towards cellular autonomy.

Russell, 2006

From the physical point of view the onset of life by the hydrothermal systems or in the hot ocean seems to be a plausible hypothesis because of the factors such as:

- electron-rich environment- electrochemical gradients- abundance of metal ions - molecular hydrogen and its volatile compounds

Sources of hydrogen on early EarthSources of hydrogen on early Earth

Kadik A.A. & Litvin Yu.A. (2007):

… the first stages of the core growth took place under reduced conditions imposed by the pristine terrestrial materials and was accompanied by the emission of CH4, H2, NH3 and minor H2O into the atmosphere.

According to Galimov (1985, 2004) the great bulk (95%) of the metal core was formed during the first 100 Ma after the accretion of the planet.

Sources of hydrogen on early EarthSources of hydrogen on early Earth

the degassing of the mantle that released the neutral or slightly acidic fluids saturated with H2, CH4, H2S, and CO2;

the serpentinization, reaction of the rocks, rich with olivine and pyroxene, with water.

photolysis of water by UV light

radiolysis, radiation-induced dissociation of H2O (background radiation on early Earth could be much higher than at present, mostly due to the decay of the short-lived isotopes.

Serpentinization — the reaction of olivine- and pyroxene-rich rocks with water at temperature 200-400°С — produces magnetite, hydroxide, and serpentine minerals, and liberates molecular hydrogen, a source of energy and electrons that can be readily utilized by a broad array of chemosynthetic organisms.

Schulte et al., 2006

Serpentinization: olivine and pyroxene are altered into serpentine minerals:

Fe2SiO4 + 5Mg2SiO4 + 9H2O 3Mg3Si2O5(OH)4 + Mg(OH)2 + 2Fe(OH)2. (1)fayalite + forsterite + water serpentine + brucite + iron hydroxidewhere fayalite and forsterite are the olivine solidsolution end-members, andMg2SiO4 + MgSiO3 + 2H2O Mg3Si2O5(OH)4 (2)forsterite + pyroxene + water serpentineThe reduced iron from the fayalite component of olivine (Reaction 1) may then be Oxidized to magnetite through the reduction of water to molecular hydrogen through the reaction

3Fe(OH)2 Fe3O4 + 2H2O + H2 (3)iron hydroxide magnetite + water + hydrogen

Schulte et al., 2006

Sources of hydrogen on early EarthSources of hydrogen on early Earth

Calculations by Tian F. et al. (2005) demonstrate that hydrogen could make up to 30% of ancient atmosphere.

The concentration of H2 in the prebiotic atmosphere was 3-4 orders of magnitude higher than at present (Hoehler, 2005).

Sources of hydrogen on early EarthSources of hydrogen on early Earth

Concentration of hydrogen could be even greater among the dissolved gases in the fluids going through the rocks and sediments due to slow migration of the fluids.

Abundance of hydrogen gave an easy access to the protons and electrons, the very motor of the cellular energy machine.

HydrogenasesHydrogenases

TheThesese enzyme enzymess catalyze the catalyze the simplestsimplest of chemical reactionsof chemical reactions::

the reversible reductive formationthe reversible reductive formation

of hydrogen from protons and of hydrogen from protons and electrons:electrons:

2H2H+ + ++ 2e 2e-- H H22

The water-gas shift reaction, an organometallic reactionsequence that is catalysed by Fe-Ni dehydrogenase, may also be one of the oldest on Earth.

Ragsdale, 2004

The structure of CpI hydrogenase from Clostridium pasteurianum

with its naturally embedded metallo-clusters.

Arrows show the pathways for the electrons, hydrogen ions, and

the hydrogen product to and from the active H-cluster.

Iron hydrogenases:Prosthetic group features

http://metallo.scripps.edu/PROMISE/MAIN.html

Prosthetic groups in largesubunits

Prosthetic groups in smallsubunits

Nickel-iron hydrogenases

Similarity of the molecular Similarity of the molecular structures: structures: a - mineral greigite a - mineral greigite ((FeFe55NiNiSS88)), ,

b -thiocubane unite of the b -thiocubane unite of the ferredoxine protein, ferredoxine protein, c - the cuboidal complex in the c - the cuboidal complex in the active site of the enzyme active site of the enzyme acetyl-CoA synthasa/carbon acetyl-CoA synthasa/carbon monoxide dehydrogenase monoxide dehydrogenase (shown simplified), and (shown simplified), and d - A-cluster of the latter.d - A-cluster of the latter.

Atoms: Fe – red, Ni – green, Atoms: Fe – red, Ni – green, S – yellow, C – grey, N – blue. S – yellow, C – grey, N – blue. R – links through sulfur to the R – links through sulfur to the reminder of the protein.reminder of the protein. After Russell, 2006After Russell, 2006

Abundant:Abundant: FeFe2+2+, Ni, Ni2+2+, Mn, Mn2+2+, Mo, Mo6+6+, V, V4+4+, W, W6+6+ etc. etc.(Frausto da Silva& Williams, 1997)(Frausto da Silva& Williams, 1997)

HOWEVER: The chemical and physical parameters HOWEVER: The chemical and physical parameters of biosphere irreversibly departed from the initial of biosphere irreversibly departed from the initial conditions.conditions.

MAJOR CHANGES: Global temperature decline, MAJOR CHANGES: Global temperature decline, oxygenation, and decreasing availability of oxygenation, and decreasing availability of hydrogen and some metals.hydrogen and some metals.

Metals in The Early OceansMetals in The Early Oceans

Geochemical evolution of magmatism between 3.5 and 2.7 Ga:

At the early stage of their development, tholeiitic magmas were considerably enriched in chalcophile and siderophile elements Fe, Mg, Cr, Ni, Co, V, Cu, and Zn.

At the next stage, calc-alkaline volcanics of greenstone belts and syntectonic TTG granitoids were enriched in lithophile elements Rb, Cs, Ba, Th, U, Pb, Nb, La, Sr, Be and others (Samsonov, Larionova, 2006).

Lead isotope compositions of tungsten-bearing minerals occurrences worldwide indicate that tungsten (W) of crustal mineralization was mainly supplied by the mantle between 3.0 and 2.4 Ga (Chiaradia, 2003).

A decline of dissolved Ni concentrations in sea water through time reduced the bioproduction of methane and affected other kinds of hydrogen metabolism

Konhauser et al., 2009

Ni

Atmosphere history(Kasting, Pavlov, 2001)

Availability change for some elements in the ocean due to its oxygenation(Williams,Frausto da Silva, 1996)

Range of MIF of sulphur over time. The great oxidation event occurred ~2.45 billion years ago. The pink bar shows the range of variability in Δ33S that is due to mass-dependent effects, indicating only small variations during the past 2.32 billion years (Kump, 2008).

Glass et al.,2009

Solubility of some metal hydroxides and metal sulfides in modern ocean (Di Toro et al., 2001)

Kirschvink J.L., 2004.

Largest ore deposits of Mn and Fe in Early Proterozoic was causes by active oxygenation of ocean water due to the photosynthesis of cyanobacteria and increasing circulation of cooling waters.

Mn

Fe

Iron formation: the sedimentary product of a complex interplay among mantle, tectonic, oceanic, and biospheric processes

Bekker et al., 2010

The age distribution of relative volumes of juvenile continental crust (Condie, 2005), and of crystallization ages for over 7000 detrital zircons (Campbell and Allen, 2008).

The peaks in the zircon crystallization ages are similar to the agesof supercontinents.

The crust generation rate curve illustrates a model inwhich the volume of new crust generated decreases with decreasing age.

Hawkesworth et al., 2010

Two major systems of nutrirent supply in the ocean ecosystem

First, mid-oceanic ridge where circulating seawater transports nutrients from MORB (mid oceanic ridge basalt) crust

Second, the Earth's surface erosion that is probably 1012 times more powerful than the first nutrient supply system (Maruyama et al., 2013)

A)Temporal trends in Mo concentrations in anoxic organic rich black shales. B) Temporal trends in Mo/TOC ratios in anoxic black shales (Wallis, 2006; Och, 2011).

A) A compilation of Vanadium concentrations in black shalesB) V/TOC ratios greatly increase across the Precambrian–Cambrian boundary whereby the highest values (exceeding 1000) are exclusivelyfrom black shales sampled in South China (Och, Shields-Zhou, 2012)

The chemistry of manganese ores through time:a signal of increasing diversity of Earth-surface environments(Maynard, 2010)

Mn

Hypothetical sequence of the incorporation of the metals intothe enzymatic evolution in the early history of the biosphere(Fedonkin, 2003, 2005).

Oxygenation of the environmentsdramatically reduced availability of some metals (such as W, V, Ni, Fe), while others (such as Mo, Cu, Zn) became more readily available.

Replacement of the unavailable metals with those available seems to be a major way in early evolutionof enzymes.

Geological Time

Oxy

gen

METAL COFACTORSOF ENZYMES

H2-related evolution

All sources of hydrogen declined in time.

The subsequent evolution of life was in a great extent driven by the competition for access to hydrogen.

Decline of the primary sources of hydrogen made life to switch for the hydrogen compounds such as H2S, CH4, NH3, and at last, H2O in the oxygenic photosynthesis.

The length of the thick arrows indicates the amount of energy released.

(Lane, 2006)

2.7 Ga ago ?

> 4 Ga ago

Time

(Lane, 2006)

H2-related evolution

H2-related evolution

By-products of the biochemical reactions related to the hydrogen uptake could be the factor of historical change in the atmosphere chemistry, in particular, the rising content of nitrogen and oxygen.

The biogeochemical cycles of macroelements (C, N, P and Si) are modulated by trace metals (J.T.Cullen et al., 1995)

Decreasing availability of hydrogen and some metals as well as the oxygenation of the habitats in the Archean-Proterozoic oceans were the major driving forces for evolution of the metabolic pathways and biological complexity of the cell.

Biological consequencesBiological consequences

Biological consequencesBiological consequences

Compartmentalization of internal environment in the cell (membranes, vesicles, organelles) that keeps the Archean biochemistry intact

Mechanisms of scavenging, concentration and storage of the metals internally

Integration of the complementary metabolic types in the cell

Biological consequencesBiological consequences

Symbiosis of the prokaryotic cells mutually dependent on each others' waste products gave the rise of the eukaryotes

Increasing rates of the biological recycling of nutrients in the ecosystem

Shift towards the heterotrophy because of need to acquire nutrients in chemically impoverished environment

Modern approach to thesymbiogenesis problemfollows the principles ofecosystem ecology andsyntrophy:

Symbiogenetic originof the eukaryotic cellwas a long process of a functional optimizationand structural miniaturization of theprimary prokaryoticecosystems in responseto the irreversible change of theenvironmental parameters.

O2 utilizing gene birth over time (David and Alm, 2010).

David and Alm, 2010

Acknowledgements:

Program of the Presidium of the Russian Academy of Sciences (‘‘Problem of the Origin of the Earth’s Biosphere and Its Evolution’’), Russian Foundation for Basic Research

Thank you for your attention!